Cited by 289Dementia and Cognitive Impairment ResearchAlzheimer's disease research and treatmentsFunctional Brain Connectivity Studies

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Neuroimaging biomarkers for Alzheimer’s disease.

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Márquez, Freddie, Yassa, Michael A.·2019·Molecular Neurodegeneration

DOI 10.1186/s13024-019-0325-5PMC PMC6555939

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Abstract

Currently, over five million Americans suffer with Alzheimer's disease (AD). In the absence of a cure, this number could increase to 13.8 million by 2050. A critical goal of biomedical research is to establish indicators of AD during the preclinical stage (i.e. biomarkers) allowing for early diagnosis and intervention. Numerous advances have been made in developing biomarkers for AD using neuroimaging approaches. These approaches offer tremendous versatility in terms of targeting distinct age-related and pathophysiological mechanisms such as structural decline (e.g. volumetry, cortical thinning), functional decline (e.g. fMRI activity, network correlations), connectivity decline (e.g. diffusion anisotropy), and pathological aggregates (e.g. amyloid and tau PET). In this review, we survey the state of the literature on neuroimaging approaches to developing novel biomarkers for the amnestic form of AD, with an emphasis on combining approaches into multimodal biomarkers. We also discuss emerging methods including imaging epigenetics, neuroinflammation, and synaptic integrity using PET tracers. Finally, we review the complementary information that neuroimaging biomarkers provide, which highlights the potential utility of composite biomarkers as suitable outcome measures for proof-of-concept clinical trials with experimental therapeutics.

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Synthesis and Preclinical Evaluation of 11 C-UCB-J as a PET Tracer for Imaging the Synaptic Vesicle Glycoprotein 2A in the Brain
Nabulsi, N. B., Mercier, J., Holden, D., Carré, S., Najafzadeh, S., Vandergeten, M.-C., Lin, S.-F., Deo, A., Price, N., Wood, M., et al. (2016) · Journal of Nuclear Medicine · doi:10.2967/jnumed.115.168179 · Cited by 296 · cited 4×
“The recent development of the SV2A PET radiotracer [(11)C] UCB-J [180] may offer the possibility of imaging synaptic density in vivo, and potentially inform biomarker science not just for AD but for numerous other conditions involving synapse loss [181].”
BackgroundInfluential
Amyloid and APOE ε4 interact to influence short-term decline in preclinical Alzheimer disease
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Synaptic Tau Seeding Precedes Tau Pathology in Human Alzheimer’s Disease Brain
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Preclinical Characterization of 18 F-MK-6240, a Promising PET Tracer for In Vivo Quantification of Human Neurofibrillary Tangles
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“Second generation tracers, such as [(18)F] MK6240 fare better in terms of off-target binding, but largescale studies with these tracers are still lacking [49].”
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Shrinkage of the Entorhinal Cortex over Five Years Predicts Memory Performance in Healthy Adults
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“clusters positively correlated between levels of microglial activation and tau aggregation via [(18)F]-AV1451 PET imaging in MCI and AD subjects [169].”
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Prediction of Alzheimer's disease in subjects with mild cognitive impairment from the ADNI cohort using patterns of cortical thinning
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Gender Modulates the APOE 4 Effect in Healthy Older Adults: Convergent Evidence from Functional Brain Connectivity and Spinal Fluid Tau Levels
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Neuronal changes in normal human aging and Alzheimer's disease.
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Early DAT is distinguished from aging by high-dimensional mapping of the hippocampus
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Age‐Related White Matter Atrophy in the Human Brain
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Functional MRI Studies of Associative Encoding in Normal Aging, Mild Cognitive Impairment, and Alzheimer's Disease
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Selective effect of age, Apo e4, and Alzheimer's disease on hippocampal subfields
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The effects of aging on area 46 of the frontal cortex of the rhesus monkey.
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Fluorodeoxyglucose–Positron-Emission Tomography, Single-Photon Emission Tomography, and Structural MR Imaging for Prediction of Rapid Conversion to Alzheimer Disease in Patients with Mild Cognitive Impairment: A Meta-Analysis
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Functional Imbalance of Anterolateral Entorhinal Cortex and Hippocampal Dentate/CA3 Underlies Age-Related Object Pattern Separation Deficits
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Self-citation
Posterior cingulate cortex atrophy and regional cingulum disruption in mild cognitive impairment and Alzheimer’s disease
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Voxel-based detection of white matter abnormalities in mild Alzheimer disease
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Hippocampal disconnection contributes to memory dysfunction in individuals at risk for Alzheimer’s disease
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Distinct binding of PET ligands PBB3 and AV-1451 to tau fibril strains in neurodegenerative tauopathies
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“Despite its many advantages, [(18)F]-1451 and similar tracers appear to bind to some dense core plaques [46], melanin-containing structures [47, 48], and minimal binding to TDP-43 [47].”
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Diffusion tensor imaging: background, potential, and utility in psychiatric research.
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In Vivo Tau, Amyloid, and Gray Matter Profiles in the Aging Brain
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Effects of Fornix Transection upon Associative Memory in Monkeys: Role of the Hippocampus in Learned Action
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In vivo changes in microglial activation and amyloid deposits in brain regions with hypometabolism in Alzheimer’s disease
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Multivariate network analysis of fiber tract integrity in Alzheimer’s disease
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Carbon 11–Labeled Pittsburgh Compound B and Carbon 11–Labeled (R)-PK11195 Positron Emission Tomographic Imaging in Alzheimer Disease
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A harmonized segmentation protocol for hippocampal and parahippocampal subregions: Why do we need one and what are the key goals?
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Alzheimer's Disease Neurodegenerative Biomarkers Are Associated with Decreased Cognitive Function but Not β-Amyloid in Cognitively Normal Older Individuals
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Memory Impairment in Aged Primates Is Associated with Focal Death of Cortical Neurons and Atrophy of Subcortical Neurons
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Amyloid-β–Associated Clinical Decline Occurs Only in the Presence of Elevated P-tau
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Subthreshold Amyloid Predicts Tau Deposition in Aging
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Neuron number in the parahippocampal region is preserved in aged rats with spatial learning deficits.
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Cortical atrophy in patients with cerebral amyloid angiopathy: a case-control study
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Hippocampal volume losses in minimally impaired elderly.
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Amyloid‐β associated volume loss occurs only in the presence of phospho‐tau
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Hippocampal activation is associated with longitudinal amyloid accumulation and cognitive decline
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“Recent evidence also suggests that hippocampal activation is associated with longitudinal amyloid accumulation and cognitive decline [74].”
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Hilar interneuron vulnerability distinguishes aged rats with memory impairment
Spiegel, A. M., Koh, M. T., Vogt, N. M., Rapp, P. R., & Gallagher, M. (2013) · The Journal of Comparative Neurology · doi:10.1002/cne.23367 · Cited by 117
Perturbations of neural circuitry in aging, mild cognitive impairment, and Alzheimer's disease
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Self-citation
Flutriciclamide (18F-GE180) PET: First-in-Human PET Study of Novel Third-Generation In Vivo Marker of Human Translocator Protein
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Prevalence, incidence and duration of Braak's stages in the general population: can we know?
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Examining the gateway to the limbic system with diffusion tensor imaging: The perforant pathway in dementia
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Insights into neuroepigenetics through human histone deacetylase PET imaging
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Tau and amyloid β proteins distinctively associate to functional network changes in the aging brain
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Multi-structure network shape analysis via normal surface momentum maps
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Temporal Sequence of Alzheimer’s Disease-Related Pathology
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Capillary cerebral amyloid angiopathy in Alzheimer’s disease: association with allocortical/hippocampal microinfarcts and cognitive decline
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Amyloid Deposition Is Linked to Aberrant Entorhinal Activity among Cognitively Normal Older Adults
Huijbers, W., Mormino, E. C., Wigman, S. E., Ward, A. M., Vannini, P., McLaren, D. G., Becker, J. A., Schultz, A. P., Hedden, T., Johnson, K. A., et al. (2014) · Journal of Neuroscience · doi:10.1523/jneurosci.3579-13.2014 · Cited by 91
Differential Associations Between Entorhinal and Hippocampal Volumes and Memory Performance in Older Adults.
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Limbic Tract Integrity Contributes to Pattern Separation Performance Across the Lifespan
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Quantitative assessment of the density of neurofibrillary tangles and senile plaques in senile dementia of the Alzheimer type. Comparison of immunocytochemistry with a specific antibody and Bodian’s protargol method.
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Atrophy is associated with posterior cingulate white matter disruption in dementia with Lewy bodies and Alzheimer’s disease
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In vivo Imaging of Glial Activation in Alzheimer's Disease
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Amnesia for Complex Naturalistic Scenes and for Objects Following Fornix Transection in the Rhesus Monkey
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APOE ε4 worsens hippocampal CA1 apical neuropil atrophy and episodic memory
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Unbiased comparison of sample size estimates from longitudinal structural measures in ADNI
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Mathematical methods for diffusion MRI processing
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Selective Disruption of the Cerebral Neocortex in Alzheimer's Disease
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Hippocampal atrophy in early Alzheimer's Disease: Anatomic specificity and validation
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Kinetic analysis of the translocator protein positron emission tomography ligand [18F]GE-180 in the human brain
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Test-retest reproducibility for the tau PET imaging agent flortaucipir F 18.
Devous, M. D., Joshi, A. D., Navitsky, M., Southekal, S., Pontecorvo, M. J., Shen, H., Lu, M., Shankle, W. R., Seibyl, J. P., Marek, K., et al. (2018) · Journal of Nuclear Medicine · doi:10.2967/jnumed.117.200691 · Cited by 79 · cited 1×
“92 across all regions tested, which indicates high test-retest reliability and suggests that this method can be used to detect changes in tau burden over time [45].”
Method
Individual differences in associative memory among older adults explained by hippocampal subfield structure and function
Carr, V. A., Bernstein, J. D., Favila, S. E., Rutt, B. K., Kerchner, G. A., & Wagner, A. D. (2017) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1713308114 · Cited by 76
Enrichment and Stratification for Predementia Alzheimer Disease Clinical Trials
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Authors: Márquez, F., & Yassa, M. A.
Affiliations: University of California, Irvine (US)
Corresponding author: Márquez, Freddie
Yassa, Michael A.
ORCID: Márquez, Freddie
Yassa, Michael A.
Venue: Molecular Neurodegeneration
Publisher: Springer Science and Business Media LLC
Published: 2019-06-07
Volume: 14
Issue: 1
Pages: 21-21
ISSN: 1750-1326 (ISSN-L)
DOI: 10.1186/s13024-019-0325-5
PMC: PMC6555939
OpenAlex: W2955418937
Cited by: 289
References: 196
Citations by year: 2026: 31 · 2025: 51 · 2024: 53 · 2023: 36 · 2022: 49 · 2021: 46 · 2020: 18 · 2019: 3
FWCI: 4.88
Type: journal article
Language: en
Open access: gold
doi.org
Licence: cc-by
creativecommons.org/licenses/by/4.0/ (tdm)
creativecommons.org/licenses/by/4.0/ (vor)
Locations: Molecular Neurodegeneration (publishedVersion, cc-by)
PubMed Central (publishedVersion, cc-by)
PubMed (publishedVersion)
eScholarship (California Digital Library) (submittedVersion, cc-by)
DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion, cc-by-sa)
Funders: Division of Molecular and Cellular Biosciences (GRFP DGE-1321846, B2D 1612490)
National Institute on Aging (P50AG05146, R21AG049220, R01AG053555)
Topics: Health Sciences › Medicine › Psychiatry and Mental health › Dementia and Cognitive Impairment Research
Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Alzheimer's disease research and treatments
Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
Keywords: Alzheimer's disease, neuroimaging biomarkers, preclinical Alzheimer's disease, early diagnosis, multimodal biomarkers, amyloid PET, tau PET, cortical thinning, brain volumetry, functional connectivity, diffusion anisotropy, neuroinflammation, synaptic integrity, composite biomarker, clinical trial outcome measures
MeSH terms: Alzheimer Disease, Brain, Humans, Biomarkers, Early Diagnosis, Amyloidogenic Proteins, Neuroimaging

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Neuroimaging biomarkers for Alzheimer’s disease.

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